ENHANCED TOLERANCE TO LOW TEMPERATURE IN TOBACCO (NICOTIANA TABACUM L.) SPRAYED WITH A LOW-TEMPERATURE-RESISTANT AGENT
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- 英文论文题名：ENHANCED TOLERANCE TO LOW TEMPERATURE IN TOBACCO (NICOTIANA TABACUM L.) SPRAYED WITH A LOW-TEMPERATURE-RESISTANT AGENT
- 论文作者：JIAN-HUA YI ; YUE LI ; ZE-MING DAI ; ZHI-HONG JIA ; WEN-XUAN PU ; ZAI-JUN SUN ; YAO-FU WANG ; HONG SHEN
- 英文论文作者：JIAN-HUA YI ; YUE LI ; ZE-MING DAI ; ZHI-HONG JIA ; WEN-XUAN PU ; ZAI-JUN SUN ; YAO-FU WANG ; HONG SHEN ; Laboratory of Root Layer Control ; College of Resources and Environment ; South China Agricultural University ; China Tobacco Hunan Industrial Co.Ltd.
- 年：2016
- 作者机构：Laboratory of Root Layer Control, College of Resources and Environment, South China Agricultural University;China Tobacco Hunan Industrial Co.Ltd.;
- 会议召开时间：2016-12-01
- 会议录名称：中国烟草学会2016年度优秀论文汇编——烟草农业主题
- 语种：英文
- 分类号：S572
- 学会代码：ZGYG
- 学会名称：中国烟草学会
- 页数：12
- 文件大小：327k
- 原文格式：D
摘要
Low-temperature stress is an important limiting factor to tobacco growth in early spring of south China. In this study, a low-temperature-resistant agent(LTRA) was employed to examine its ameliorating effect on the inhibition of tobacco growth triggered by low-temperature stress. Results indicated that low-temperature stress of 12 °C for 6 days reduced root number and biomass of tobacco seedling by 27.4% and 24.1%,while treatment with LTRA could recover the inhibitory effect of low-temperature stress on tobacco growth significantly. The content of ascorbic acid and the activities of superoxide dismutase and catalase at lowtemperature stress were 65.2%, 53.5% and 32.1% of those at normal temperature condition(26 °C), while the corresponding values with LTRA treatment were 89.2%, 88.9% and 74.2%, suggesting that LTRA treatment could enhance the activity of antioxidant enzyme and the synthesis of antioxidant compounds.Low-temperature stress increased the membrane permeability by 84.8%, while LTRA treatment recovered it by 77.4%. Furthermore, LTRA treatment contributed to increase chlorophyll synthesis and maintain the integrity of tobacco leaf structure. Effective component analysis indicated that the complex of ammonium calcium nitrate and glycine betaine was the main effective component of LTRA in maintaining membrane integrity. Its effective concentration was 1.0 g L~(-1). The above results suggested that LTRA could enhance the synthesis of chlorophyll, activate the activity of antioxidant enzyme, maintain the integrity of cell membrane, and thus elevate the tolerance of tobacco seedlings to low-temperature stress.
Low-temperature stress is an important limiting factor to tobacco growth in early spring of south China. In this study, a low-temperature-resistant agent(LTRA) was employed to examine its ameliorating effect on the inhibition of tobacco growth triggered by low-temperature stress. Results indicated that low-temperature stress of 12 °C for 6 days reduced root number and biomass of tobacco seedling by 27.4% and 24.1%,while treatment with LTRA could recover the inhibitory effect of low-temperature stress on tobacco growth significantly. The content of ascorbic acid and the activities of superoxide dismutase and catalase at lowtemperature stress were 65.2%, 53.5% and 32.1% of those at normal temperature condition(26 °C), while the corresponding values with LTRA treatment were 89.2%, 88.9% and 74.2%, suggesting that LTRA treatment could enhance the activity of antioxidant enzyme and the synthesis of antioxidant compounds.Low-temperature stress increased the membrane permeability by 84.8%, while LTRA treatment recovered it by 77.4%. Furthermore, LTRA treatment contributed to increase chlorophyll synthesis and maintain the integrity of tobacco leaf structure. Effective component analysis indicated that the complex of ammonium calcium nitrate and glycine betaine was the main effective component of LTRA in maintaining membrane integrity. Its effective concentration was 1.0 g L~(-1). The above results suggested that LTRA could enhance the synthesis of chlorophyll, activate the activity of antioxidant enzyme, maintain the integrity of cell membrane, and thus elevate the tolerance of tobacco seedlings to low-temperature stress.
Low-temperature stress is an important limiting factor to tobacco growth in early spring of south China. In this study, a low-temperature-resistant agent(LTRA) was employed to examine its ameliorating effect on the inhibition of tobacco growth triggered by low-temperature stress. Results indicated that low-temperature stress of 12 °C for 6 days reduced root number and biomass of tobacco seedling by 27.4% and 24.1%,while treatment with LTRA could recover the inhibitory effect of low-temperature stress on tobacco growth significantly. The content of ascorbic acid and the activities of superoxide dismutase and catalase at lowtemperature stress were 65.2%, 53.5% and 32.1% of those at normal temperature condition(26 °C), while the corresponding values with LTRA treatment were 89.2%, 88.9% and 74.2%, suggesting that LTRA treatment could enhance the activity of antioxidant enzyme and the synthesis of antioxidant compounds.Low-temperature stress increased the membrane permeability by 84.8%, while LTRA treatment recovered it by 77.4%. Furthermore, LTRA treatment contributed to increase chlorophyll synthesis and maintain the integrity of tobacco leaf structure. Effective component analysis indicated that the complex of ammonium calcium nitrate and glycine betaine was the main effective component of LTRA in maintaining membrane integrity. Its effective concentration was 1.0 g L~(-1). The above results suggested that LTRA could enhance the synthesis of chlorophyll, activate the activity of antioxidant enzyme, maintain the integrity of cell membrane, and thus elevate the tolerance of tobacco seedlings to low-temperature stress.
引文
Alonso,A.,Queiroz,C.S.and Magalhaes,A.C.(1997).Chilling stress leads to increased cell membrane rigidity in roots of coffee(Coffee arabica L.)seedlings.Biochimica Biophysica Acta 1323:75-84.
Ao,P.X.,Li,Z.G.,Fan,D.M.and Gong,M.(2013).Involvement of antioxidant defense system in chill hardening induced chilling tolerance in Jatropha curcas seedlings.Acta Physiologia Plantarum 35:153-160.
Apel,K.and Hirt,H.(2004).Reactive oxygen species:metabolism,oxidative stress,and signal transduction.Annual Review of Plant Biology 55:373-399.
Caldwell,E.F.,Leib,B.G.and Savoy,H.J.(2010).Irrigation,fertilization,and plasticulture increase yield and quality while reducing carcinogen formation in burley tobacco.Applied Engineering in Agriculture 26:381-390.
Campos,P.S.,Quartin,V.,Ramalho,J.C.and Nunes,M.A.(2003).Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp.plants.Journal of Plant Physiology 160:283-292.
Deng,S.Y.,Chen,J.J.,Luo,F.M.,Wang,W.,Ling,S.J.and Wang,J.(2012).Effects of exogenous salicylic acid on antioxidant metabolism of flue-cured tobacco under low temperature stress.Tobacco Science and Technology 2:71-74.(in Chinese).
Dias,M.A.and Costa,M.M.(1983).Effect of low salt concentrations on nitrate reductase and peroxidase of sugar beet leaves.Journal of Experimental Botany 34:537-543.
Fan,W.,Zhang,M.,Zhang,H.and Zhang,P.(2012).Improved tolerance to various abiotic stresses in transgenic sweet potato(Ipomoea batatas)expressing spinach betaine aldehyde dehydrogenase.PLo S One 7:e37344.
Hara,M.,Terashima,S.,Fukaya,T.and Kuboi,T.(2003).Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco.Planta 217:290-298.
Heidarvand,L.,Amiri,R.M.and Naghavi,M.R.(2011).Physiological and morphological characteristics of chickpea accessions under low temperature stress.Russian Journal of Plant Physiology 58:157-163.
Hendrickson,L.,Ball,M.C.,Wood,J.T.,Chow,W.S.and Furbank,R.T.(2004).Low temperature effects on photosynthesis and growth of grapevine.Plant and Cell Environment 27:795-809.
Holmstrom,K.O.,Somersalo,S.,Mandal,A.,Palva,T.E.and Welin,B.(2000).Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine.Journal of Experimental Botany 51:177-185.
Huang,Y.,He,X.L.,Zhang,W.and Zhou,J.(2012).Microstructure differentiation of middle leaves among flue-cured tobacco cultivars.Tobacco Science and Technology 299:76-79.(in Chinese).
James,F.D.,Humberto,L.D.,Christine,H.F.and Ian,M.S.(2000).Effect of salicylic acid on oxidative stress and thermotolerance in tobacco.Journal of Plant Physiology 156:659-665.
Jennings,P.and Saltveit,M.E.(1994).Temperature and chemical shocks induce chilling tolerance in germinating Cucumis sativus(cv.Poinsett 76)seeds.Physiologia Plantarum 91:703-707.
Kang,G.Z.,Wang,C.H.,Sun,G.C.and Wang,Z.X.(2003).Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling to tolerance of banana seedlings.Environmental and Experimental Botany 50:9-15.
Karabudak,M.,Bor,M.,?zdemir,F.and Türkan,˙I.(2014).Glycine betaine protects tomato(Solanum lycopersicum)plants at low temperature by inducing fatty acid desaturase7 and lipoxygenase gene expression.Molecular Biology Reports 41:1401-1410.
Kato,M.and Shimizu,S.(1987).Chlorophyll metabolism in higher plants VII.Chlorophyll degradation in senescing tobacco leaves:phenolic-dependent peroxidative degradation.Canadian Journal of Botany 65:729-735.
Kim,Y.-H.,Bae,J.M.and Huh,G.-H.(2010).Transcriptional regulation of the cinnamyl alcohol dehydrogenase gene from sweetpotato in response to plant developmental stage and environmental stress.Plant Cell Reports 29:779-791.
Kocsy,G.,Pal,M.,Soltesz,A.,Szalai,G.,Boldizsar,A.,Kovacs,V.and Janda,T.(2011).Low temperature and oxidative stress in cereals.Acta Agronomica Hungarica 59:25-36.
Liu,G.S.(2003).Tobacco Cultivation.Beijing,China:China Agriculture Press.(in Chinese).
Liu,H.X.,Zeng,S.X.,Wang,Y.R.,Li,P.,Chen,D.F.and Guo,J.Y.(1985).Effect of low temperature on superoxidase in leaf cells of different chilling-resistant cucumber species.Acta Phytophysiologica Sinica 11:48-57.(in Chinese).
Liu,R.M.,Hu,G.F.,Wei,Q.,Wang,W.C.,Li,F.L.and Hu,B.Z.(2010).Effect of low temperature on chloroplast ultra-structure and physiological characteristics of transferring CBF3 gene tobacco seedling.Journal of Anhui Agricultural Science 38:9501-9503.(in Chinese).
Los,D.A.and Murata,N.(1998).Structure and expression of fatty acid desaturases.Biochimica et Biophysica Acta1394:3-15.
Ouyang,S.Q.,He,S.J.and Liu,P.(2011).The role of tocopherol cyclase in salt stress tolerance of rice(Oryza sativa).Science China-Life Science 54:181-188.
Popov,V.N.,Antipina,O.V.and Trunova,T.I.(2010).Lipid peroxidation during low-temperature adaptation of cold-sensitive tobacco leaves and roots.Russian Journal of Plant Physiology 57:144-147.
Parvanova,D.,Ivanov,S.,Konstantinova,T.,Karanov,E.,Atanassov,A.,Tsvetkov,T.,Alexieva,V.and Djilianov,D.(2004).Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress.Plant Physiology and Biochemistry 42:57-63.
Prasad,T.K.,Anderson,M.D.,Martin,B.A.and Stewart,C.R.(1994).Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide.The Plant Cell 6:65-74.
Raese,J.T.(1997).Cold tolerance,yield,and fruit quality of‘d’Anjou’pears influenced by nitrogen fertilizer rates and time of application.Journal of Plant Nutrition 20:1007-1025.
Singh,N.,Mishra,A.and Jha,B.(2014).Over-expression of the peroxisomal ascorbate peroxidase(Sbp APX)gene cloned from halophyte salicornia brachiata confers salt and drought stress tolerance in transgenic tobacco.Marine Biotechnology 16:321-332.
Miura,K.and Tada,Y.(2014).Regulation of water,salinity,and cold stress responses by salicylic acid.Frontiers in Plant Science 5(4):1-12.
Mutlu,S.,Karada?go?glu,?.,Atici,?.and Nalbantoglu,B.(2013).Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast.Biologia Plantarum 57:507-513.
Thounaojam,T.C.,Panda,P.,Mazumdar,P.,Kumar,D.,Sharma,G.D.,Sahoo,L.and Panda,S.K.(2012).Excess copper induced oxidative stress and response of antioxidants in rice.Plant Physiology and Biochemistry 53:33-39.
Wang,C.,Ma,X.L.,Hui,Z.and Wang,W.(2008).Glycine betaine improves thylakoid membrane function of tobacco leaves under low-temperature stress.Photosynthetica 46:254-258.
Wang,X.M.,Chen,X.F.,Wang,Z.,Nikolay,D.,Vladimir,C.and Gao,H.W.(2010).Isolation and characterization of Go DREB encoding an ERF-type protein in forage legume Galegae orientalis.Genes and Genetic Systems 85:157-166.
Wani,S.H.,Singh,N.B.,Naorem,B.,Haribhushan,A.and Mir,J.I.(2013).Compatible solute engineering in plants for abiotic stress tolerance-Role of glycine betaine.Current Genomics 14:157-165.
Wei,W.,Zhang,Y.X.,Han,L.,Guan,Z.Q.and Chai,T.Y.(2008).A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco.Plant Cell Reports 27:795-803.
Xu,S.C.,Li,Y.P.,Hu,J.,Guan,Y.J.,Ma,W.G.,Zheng,Y.Y.and Zhu,S.J.(2010).Responses of antioxidant enzymes to chilling stress in tobacco seedlings.Agricultural Sciences in China 9:1594-1601.
Zhang,W.P.,Jiang,B.,Lou,L.N.,Lu,M.H.,Yang,M.and Chen,J.F.(2011).Impact of salicylic acid on the antioxidant enzyme system and hydrogen peroxide production in Cucumis sativus under chilling stress.Zeitschrift fur Naturfoschung C 66:413-432.
Zhang,X.-Y.,Liang,C.,Wang,G.-P.,Luo,Y.and Wang,W.(2010).The protection of wheat plasma membrane under cold stress by glycine betaine overproduction.Biologia Plantarum 54:83-88.
Zhang,Y.P.,Jia,F.F.,Zhang,X.M.,Qiao,Y.X.,Shi,K.,Zhou,Y.H.and Yu,J.Q.(2012).Temperature effects on the reactive oxygen species formation and antioxidant defense in roots of two cucurbit species with contrasting root zone temperature optima.Acta Physiologiae Plantarum 34:713-720.
Ao,P.X.,Li,Z.G.,Fan,D.M.and Gong,M.(2013).Involvement of antioxidant defense system in chill hardening induced chilling tolerance in Jatropha curcas seedlings.Acta Physiologia Plantarum 35:153-160.
Apel,K.and Hirt,H.(2004).Reactive oxygen species:metabolism,oxidative stress,and signal transduction.Annual Review of Plant Biology 55:373-399.
Caldwell,E.F.,Leib,B.G.and Savoy,H.J.(2010).Irrigation,fertilization,and plasticulture increase yield and quality while reducing carcinogen formation in burley tobacco.Applied Engineering in Agriculture 26:381-390.
Campos,P.S.,Quartin,V.,Ramalho,J.C.and Nunes,M.A.(2003).Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp.plants.Journal of Plant Physiology 160:283-292.
Deng,S.Y.,Chen,J.J.,Luo,F.M.,Wang,W.,Ling,S.J.and Wang,J.(2012).Effects of exogenous salicylic acid on antioxidant metabolism of flue-cured tobacco under low temperature stress.Tobacco Science and Technology 2:71-74.(in Chinese).
Dias,M.A.and Costa,M.M.(1983).Effect of low salt concentrations on nitrate reductase and peroxidase of sugar beet leaves.Journal of Experimental Botany 34:537-543.
Fan,W.,Zhang,M.,Zhang,H.and Zhang,P.(2012).Improved tolerance to various abiotic stresses in transgenic sweet potato(Ipomoea batatas)expressing spinach betaine aldehyde dehydrogenase.PLo S One 7:e37344.
Hara,M.,Terashima,S.,Fukaya,T.and Kuboi,T.(2003).Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco.Planta 217:290-298.
Heidarvand,L.,Amiri,R.M.and Naghavi,M.R.(2011).Physiological and morphological characteristics of chickpea accessions under low temperature stress.Russian Journal of Plant Physiology 58:157-163.
Hendrickson,L.,Ball,M.C.,Wood,J.T.,Chow,W.S.and Furbank,R.T.(2004).Low temperature effects on photosynthesis and growth of grapevine.Plant and Cell Environment 27:795-809.
Holmstrom,K.O.,Somersalo,S.,Mandal,A.,Palva,T.E.and Welin,B.(2000).Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine.Journal of Experimental Botany 51:177-185.
Huang,Y.,He,X.L.,Zhang,W.and Zhou,J.(2012).Microstructure differentiation of middle leaves among flue-cured tobacco cultivars.Tobacco Science and Technology 299:76-79.(in Chinese).
James,F.D.,Humberto,L.D.,Christine,H.F.and Ian,M.S.(2000).Effect of salicylic acid on oxidative stress and thermotolerance in tobacco.Journal of Plant Physiology 156:659-665.
Jennings,P.and Saltveit,M.E.(1994).Temperature and chemical shocks induce chilling tolerance in germinating Cucumis sativus(cv.Poinsett 76)seeds.Physiologia Plantarum 91:703-707.
Kang,G.Z.,Wang,C.H.,Sun,G.C.and Wang,Z.X.(2003).Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling to tolerance of banana seedlings.Environmental and Experimental Botany 50:9-15.
Karabudak,M.,Bor,M.,?zdemir,F.and Türkan,˙I.(2014).Glycine betaine protects tomato(Solanum lycopersicum)plants at low temperature by inducing fatty acid desaturase7 and lipoxygenase gene expression.Molecular Biology Reports 41:1401-1410.
Kato,M.and Shimizu,S.(1987).Chlorophyll metabolism in higher plants VII.Chlorophyll degradation in senescing tobacco leaves:phenolic-dependent peroxidative degradation.Canadian Journal of Botany 65:729-735.
Kim,Y.-H.,Bae,J.M.and Huh,G.-H.(2010).Transcriptional regulation of the cinnamyl alcohol dehydrogenase gene from sweetpotato in response to plant developmental stage and environmental stress.Plant Cell Reports 29:779-791.
Kocsy,G.,Pal,M.,Soltesz,A.,Szalai,G.,Boldizsar,A.,Kovacs,V.and Janda,T.(2011).Low temperature and oxidative stress in cereals.Acta Agronomica Hungarica 59:25-36.
Liu,G.S.(2003).Tobacco Cultivation.Beijing,China:China Agriculture Press.(in Chinese).
Liu,H.X.,Zeng,S.X.,Wang,Y.R.,Li,P.,Chen,D.F.and Guo,J.Y.(1985).Effect of low temperature on superoxidase in leaf cells of different chilling-resistant cucumber species.Acta Phytophysiologica Sinica 11:48-57.(in Chinese).
Liu,R.M.,Hu,G.F.,Wei,Q.,Wang,W.C.,Li,F.L.and Hu,B.Z.(2010).Effect of low temperature on chloroplast ultra-structure and physiological characteristics of transferring CBF3 gene tobacco seedling.Journal of Anhui Agricultural Science 38:9501-9503.(in Chinese).
Los,D.A.and Murata,N.(1998).Structure and expression of fatty acid desaturases.Biochimica et Biophysica Acta1394:3-15.
Ouyang,S.Q.,He,S.J.and Liu,P.(2011).The role of tocopherol cyclase in salt stress tolerance of rice(Oryza sativa).Science China-Life Science 54:181-188.
Popov,V.N.,Antipina,O.V.and Trunova,T.I.(2010).Lipid peroxidation during low-temperature adaptation of cold-sensitive tobacco leaves and roots.Russian Journal of Plant Physiology 57:144-147.
Parvanova,D.,Ivanov,S.,Konstantinova,T.,Karanov,E.,Atanassov,A.,Tsvetkov,T.,Alexieva,V.and Djilianov,D.(2004).Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress.Plant Physiology and Biochemistry 42:57-63.
Prasad,T.K.,Anderson,M.D.,Martin,B.A.and Stewart,C.R.(1994).Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide.The Plant Cell 6:65-74.
Raese,J.T.(1997).Cold tolerance,yield,and fruit quality of‘d’Anjou’pears influenced by nitrogen fertilizer rates and time of application.Journal of Plant Nutrition 20:1007-1025.
Singh,N.,Mishra,A.and Jha,B.(2014).Over-expression of the peroxisomal ascorbate peroxidase(Sbp APX)gene cloned from halophyte salicornia brachiata confers salt and drought stress tolerance in transgenic tobacco.Marine Biotechnology 16:321-332.
Miura,K.and Tada,Y.(2014).Regulation of water,salinity,and cold stress responses by salicylic acid.Frontiers in Plant Science 5(4):1-12.
Mutlu,S.,Karada?go?glu,?.,Atici,?.and Nalbantoglu,B.(2013).Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast.Biologia Plantarum 57:507-513.
Thounaojam,T.C.,Panda,P.,Mazumdar,P.,Kumar,D.,Sharma,G.D.,Sahoo,L.and Panda,S.K.(2012).Excess copper induced oxidative stress and response of antioxidants in rice.Plant Physiology and Biochemistry 53:33-39.
Wang,C.,Ma,X.L.,Hui,Z.and Wang,W.(2008).Glycine betaine improves thylakoid membrane function of tobacco leaves under low-temperature stress.Photosynthetica 46:254-258.
Wang,X.M.,Chen,X.F.,Wang,Z.,Nikolay,D.,Vladimir,C.and Gao,H.W.(2010).Isolation and characterization of Go DREB encoding an ERF-type protein in forage legume Galegae orientalis.Genes and Genetic Systems 85:157-166.
Wani,S.H.,Singh,N.B.,Naorem,B.,Haribhushan,A.and Mir,J.I.(2013).Compatible solute engineering in plants for abiotic stress tolerance-Role of glycine betaine.Current Genomics 14:157-165.
Wei,W.,Zhang,Y.X.,Han,L.,Guan,Z.Q.and Chai,T.Y.(2008).A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco.Plant Cell Reports 27:795-803.
Xu,S.C.,Li,Y.P.,Hu,J.,Guan,Y.J.,Ma,W.G.,Zheng,Y.Y.and Zhu,S.J.(2010).Responses of antioxidant enzymes to chilling stress in tobacco seedlings.Agricultural Sciences in China 9:1594-1601.
Zhang,W.P.,Jiang,B.,Lou,L.N.,Lu,M.H.,Yang,M.and Chen,J.F.(2011).Impact of salicylic acid on the antioxidant enzyme system and hydrogen peroxide production in Cucumis sativus under chilling stress.Zeitschrift fur Naturfoschung C 66:413-432.
Zhang,X.-Y.,Liang,C.,Wang,G.-P.,Luo,Y.and Wang,W.(2010).The protection of wheat plasma membrane under cold stress by glycine betaine overproduction.Biologia Plantarum 54:83-88.
Zhang,Y.P.,Jia,F.F.,Zhang,X.M.,Qiao,Y.X.,Shi,K.,Zhou,Y.H.and Yu,J.Q.(2012).Temperature effects on the reactive oxygen species formation and antioxidant defense in roots of two cucurbit species with contrasting root zone temperature optima.Acta Physiologiae Plantarum 34:713-720.